Aggressiveness has been one of the behavioral traits most examined with various standard testing methods. We used two distinct methods (the mirror and the real opponent tests) to evaluate individual aggression and relate it to the activity and individual stress of chub (Squalius cephalus L.). Three hypotheses were formulated and tested: (a) there is a significant positive relationship between the aggressiveness of individuals measured with the mirror and the real opponent tests, indicating their convergent validity; (b) the irregularities in response to the aggressiveness and activity tests lead to the context-specific expression of the behavioral syndromes; and (c) there is a significant positive relationship between the stress induced in individuals by both tests of aggressiveness, demonstrating individually consistent stress-coping strategies. The first and the second hypothesis were confirmed, while the third hypothesis was rejected. Our results suggest that particular tests of aggressiveness could act as a situation with high strength, leaving little variation between individual responses. Thus, we propose that for the proper interpretation of various studies using different tests to study identical behavioral traits, it is important to consider the convergent validity of not only the tested behavioral traits but also the individual stress responses. The chub also showed stress relieve through aggressiveness, suggesting the species as a prospective animal model to the study interaction between the stress and the aggressiveness. A detailed aggression ethogram of chub was provided to facilitate the use of this specie in future studies.

Department of Zoology and Fisheries Czech University of Life Sciences Prague Prague Suchdol Czech Republic

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Ariyomo, T. O., & Watt, P. J. (2012). The effect of variation in boldness and aggressiveness on the reproductive success of zebrafish. Animal Behaviour, 83, 41-46. https://doi.org/10.1016/j.anbehav.2011.10.004

Arnott, G., Ashton, C., & Elwood, R. W. (2011). Lateralization of lateral displays in convict cichlids. Biology Letters, 7, 683-685. https://doi.org/10.1098/rsbl.2011.0328

Arnott, G., Beattie, E., & Elwood, R. W. (2016). To breathe or fight? Siamese fighting fish differ when facing a real opponent or mirror image. Behavioural Processes, 129, 11-17. https://doi.org/10.1016/j.beproc.2016.05.005

Arnott, G., & Elwood, R. (2009). Probing aggressive motivation in a cichlid fish. Biology Letters, 5, 762-764. https://doi.org/10.1098/rsbl.2009.0526

Bakker, T. C. (1994). Genetic correlations and the control of behavior, exemplified by aggressiveness in sticklebacks. Advances in the Study of Behavior, 23, 135-171.

Balestrieri, A., Prigioni, C., Remonti, L., Sgrosso, S., & Priore, G. (2006). Feeding ecology of Leuciscus cephalus and Rutilus rubilio in southern Italy. Italian Journal of Zoology, 73, 129-135. https://doi.org/10.1080/11250000600679561

Balzarini, V., Taborsky, M., Wanner, S., Koch, F., & Frommen, J. G. (2014). Mirror, mirror on the wall: The predictive value of mirror tests for measuring aggression in fish. Behavioral Ecology and Sociobiology, 68, 871-878. https://doi.org/10.1007/s00265-014-1698-7

Baras, E., & Nindaba, J. (1998). Seasonal and diel utilisation of inshore microhabitats by larvae and juveniles of Leuciscus cephalus and Leuciscus leuciscus. Environmental Biology of Fishes, 56, 183-197.

Benus, R. F., Bohus, B., Koolhaas, J. M., & Van Oortmerssen, G. A. (1991). Heritable variation for aggression as a reflection of individual coping strategies. Experientia, 47, 1008-1019. https://doi.org/10.1007/BF01923336

Biro, P. A., & Adriaenssens, B. (2013). Predictability as a personality trait: Consistent differences in intraindividual behavioral variation. The American Naturalist, 182, 621-629. https://doi.org/10.1086/673213

Biro, P. A., Beckmann, C., & Stamps, J. A. (2009). Small within-day increases in temperature affects boldness and alters personality in coral reef fish. Proceedings of the Royal Society B: Biological Sciences, 277, 71-77. https://doi.org/10.1098/rspb.2009.1346

Boyer, N., Réale, D., Marmet, J., Pisanu, B., & Chapuis, J.-L. (2010). Personality, space use and tick load in an introduced population of Siberian chipmunks Tamias sibiricus. Journal of Animal Ecology, 79, 538-547. https://doi.org/10.1111/j.1365-2656.2010.01659.x

Brodin, T., Mikolajewski, D. J., & Johansson, F. (2006). Behavioral and life history effects of predator diet cues during ontogeny in damselfly larvae. Oecologia, 148, 162-169. https://doi.org/10.1007/s00442-005-0334-7

Budaev, S. V., Zworykin, D. D., & Mochek, A. D. (1999). Consistency of individual differences in behaviour of the lion-headed cichlid, Steatocranus casuarius. Behavioural Processes, 48, 49-55. https://doi.org/10.1016/S0376-6357(99)00068-6

Carter, A. J., Feeney, W. E., Marshall, H. H., Cowlishaw, G., & Heinsohn, R. (2013). Animal personality: What are behavioural ecologists measuring? Biological Reviews, 88, 465-475. https://doi.org/10.1111/brv.12007

Cattelan, S., Lucon-Xiccato, T., Pilastro, A., & Griggio, M. (2017). Is the mirror test a valid measure of fish sociability? Animal Behaviour, 127, 109-116. https://doi.org/10.1016/j.anbehav.2017.03.009

Chapman, D. W. (1966). Food and space as regulators of salmonid populations in streams. The American Naturalist, 100, 345-357.

Collier, A. D., Khan, K. M., Caramillo, E. M., Mohn, R. S., & Echevarria, D. J. (2014). Zebrafish and conditioned place preference: A translational model of drug reward. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 55, 16-25. https://doi.org/10.1016/j.pnpbp.2014.05.014

Colléter, M., & Brown, C. (2011). Personality traits predict hierarchy rank in male rainbowfish social groups. Animal Behaviour, 81, 1231-1237. https://doi.org/10.1016/j.anbehav.2011.03.011

Conrad, J. L., Weinersmith, K. L., Brodin, T., Saltz, J. B., & Sih, A. (2011). Behavioural syndromes in fishes: A review with implications for ecology and fisheries management. Journal of Fish Biology, 78, 395-435. https://doi.org/10.1111/j.1095-8649.2010.02874.x

Copeland, D. L., Levay, B., Sivaraman, B., Beebe-Fugloni, C., & Earley, R. L. (2011). Metabolic costs of fighting are driven by contest performance in male convict cichlid fish. Animal Behaviour, 82, 271-280. https://doi.org/10.1016/j.anbehav.2011.05.001

Cutts, C. J., Betcalfe, N. B., & Caylor, A. C. (1998). Aggression and growth depression in juvenile Atlantic salmon: The consequences of individual variation in standard metabolic rate. Journal of Fish Biology, 52, 1026-1037. https://doi.org/10.1111/j.1095-8649.1998.tb00601.x

Desjardins, J. K., & Fernald, R. D. (2010). What do fish make of mirror images? Biology Letters, 6, 744-747. https://doi.org/10.1098/rsbl.2010.0247

Dingemanse, N. J., Wright, J., Kazem, A. J., Thomas, D. K., Hickling, R., & Dawnay, N. (2007). Behavioural syndromes differ predictably between 12 populations of three-spined stickleback. Journal of Animal Ecology, 76, 1128-1138. https://doi.org/10.1111/j.1365-2656.2007.01284.x

Earley, R. L., Edwards, J. T., Aseem, O., Felton, K., Blumer, L. S., Karom, M., & Grober, M. S. (2006). Social interactions tune aggression and stress responsiveness in a territorial cichlid fish (Archocentrus nigrofasciatus). Physiology & Behavior, 88, 353-363. https://doi.org/10.1016/j.physbeh.2006.04.002

Earley, R. L., Hsu, Y., & Wolf, L. L. (2000). The use of standard aggression testing methods to predict combat behaviour and contest outcome in Rivulus marmoratus dyads (Teleostei: Cyprinodontidae). Ethology, 106, 743-761. https://doi.org/10.1046/j.1439-0310.2000.00586.x

Elwood, R. W., Stoilova, V., McDonnell, A., Earley, R. L., & Arnott, G. (2014). Do mirrors reflect reality in agonistic encounters? A test of mutual cooperation in displays. Animal Behaviour, 97, 63-67. https://doi.org/10.1016/j.anbehav.2014.07.028

Enquist, M., Leimar, O., Ljungberg, T., Mallner, Y., & Segerdahl, N. (1990). A test of the sequential assessment game: Fighting in the cichlid fish Nannacara anomala. Animal Behaviour, 40, 1-14.

Freitas, R. H., Negrão, C. A., Felício, A. K. C., & Volpato, G. L. (2014). Eye darkening as a reliable, easy and inexpensive indicator of stress in fish. Zoology, 117, 179-184. https://doi.org/10.1016/j.zool.2013.09.005

Godin, J. G., & Dugatkin, L. A. (1996). Female mating preference for bold males in the guppy, Poecilia reticulata. Proceedings of the National Academy of Sciences, 93, 10262-10267. https://doi.org/10.1073/pnas.93.19.10262

Gómez-Laplaza, L. M., & Morgan, E. (2003). The influence of social rank in the angelfish, Pterophyllum scalare, on locomotor and feeding activities in a novel environment. Laboratory Animals, 37, 108-120. https://doi.org/10.1258/00236770360563741

Holway, D. A., & Suarez, A. V. (1999). Animal behavior: An essential component of invasion biology. Trends in Ecology & Evolution, 14, 328-330. https://doi.org/10.1016/S0169-5347(99)01636-5

Honess, P. E., & Marin, C. M. (2006). Behavioural and physiological aspects of stress and aggression in nonhuman primates. Neuroscience & Biobehavioral Reviews, 30, 390-412. https://doi.org/10.1016/j.neubiorev.2005.04.003

Horký, P., Douda, K., Maciak, M., Závorka, L., & Slavík, O. (2014). Parasite-induced alterations of host behaviour in a riverine fish: the effects of glochidia on host dispersal. Freshwater Biology, 59, 1452-1461. https://doi.org/10.1111/fwb.12357

Huntingford, F., Jobling, M., & Kadri, S. (2012). Aquaculture and behavior. Iowa: Blackwell Publishing Ltd. ISBN: 9781405130899.

Kenward, M. G., & Roger, J. H. (1997). Small sample inference for fixed effects from restricted maximum likelihood. Biometrics, 53, 983-997. https://doi.org/10.2307/2533558

Kern, E. M., Robinson, D., Gass, E., Godwin, J., & Langerhans, R. B. (2016). Correlated evolution of personality, morphology and performance. Animal Behaviour, 117, 79-86. https://doi.org/10.1016/j.anbehav.2016.04.007

Koolhaas, J. M., Korte, S. M., De Boer, S. F., Van Der Vegt, B. J., Van Reenen, C. G., Hopster, H., … Blokhuis, H. J. (1999). Coping styles in animals: Current status in behavior and stress-physiology. Neuroscience & Biobehavioral Reviews, 23, 925-935. https://doi.org/10.1016/S0149-7634(99)00026-3

Kottelat, M., & Freyhof, J. (2007). Handbook of European freshwater fishes. Cornol, Switzerland: Publications Kottelat.

Krywult, M., Klich, M., & Szarek-Gwiazda, E. (2008). Metal concentrations in chub, Leuciscus cephalus, from a submontane river. Acta Ichthyologica et Piscatoria, 1, 47-53. https://doi.org/10.3750/AIP2008.38.1.08

Lahti, K., Huuskonen, H., Laurila, A., & Piironen, J. (2002). Metabolic rate and aggressiveness between Brown Trout populations. Functional Ecology, 16, 157-174. https://doi.org/10.1046/j.1365-2435.2002.00618.x

Li, C. Y., Curtis, C., & Earley, R. L. (2018). Nonreversing mirrors elicit behaviour that more accurately predicts performance against live opponents. Animal Behaviour, 137, 95-105. https://doi.org/10.1016/j.anbehav.2018.01.010

Li, C. Y., Hofmann, H. A., Harris, M. L., & Earley, R. L. (2018). Real or fake? Natural and artificial social stimuli elicit divergent behavioural and neural responses in mangrove rivulus, Kryptolebias marmoratus. Proceedings of the Royal Society B, 285(1891), 20181610. https://doi.org/10.1098/rspb.2018.1610

Logue, D. M., Takahashi, A. D., & Cade, W. H. (2011). Aggressiveness and size: A model and two tests. American Naturalist, 177, 202-210. https://doi.org/10.1086/657978

Lucas, M. C., Mercer, T., Armstrong, J. D., McGinty, S., & Rycroft, P. (1999). Use of a flat-bed passive integrated transponder antenna array to study the migration and behaviour of lowland river fishes at a fish pass. Fisheries Research, 44, 183-191. https://doi.org/10.1016/S0165-7836(99)00061-2

Maan, M. E., Groothuis, T. G., & Wittenberg, J. (2001). Escalated fighting despite predictors of conflict outcome: Solving the paradox in a South American cichlid fish. Animal Behaviour, 62, 623-634. https://doi.org/10.1006/anbe.2001.1819

Maillet, Z., Halliday, W. D., & Blouin-Demers, G. (2015). Exploratory and defensive behaviours change with sex and body size in eastern garter snakes (Thamnophis sirtalis). Journal of Ethology, 33, 47-54. https://doi.org/10.1007/s10164-014-0416-2

Marković, G. (2007). A contribution to data on Chub (Leuciscus cephalus L., Cyprinidae, PISCES) diet in river conditions. Acta Agriculturae Serbica, 12, 13-18.

Mischel, W. (1973). Toward a cognitive social learning reconceptualization of personality. Psychological Review, 80, 252-283.

Moscicki, M. K., & Hurd, P. L. (2015). Sex, boldness and stress experience affect convict cichlid, Amatitlania nigrofasciata, open field behaviour. Animal Behaviour, 107, 105-114. https://doi.org/10.1016/j.anbehav.2015.05.027

Nascimento, A. L., & Gonzaga, M. O. (2016). Maternal defensive behaviors of Uloborus sp. (Araneae, Uloboridae): Behavioral repertoire and influence of clutch size and female size on female aggressiveness. Acta Ethologica, 19, 33-41. https://doi.org/10.1007/s10211-015-0220-1

Neat, F. C., Huntingford, F. A., & Beveridge, M. M. C. (1998). Fighting and assessment in male cichlid fish: The effects of asymmetries in gonadal state and body size. Animal Behaviour, 55, 883-891.

Neat, F. C., Taylor, A. C., & Huntingford, F. A. (1998). Proximate costs of fighting in male cichlid fish: The role of injuries and energy metabolism. Animal Behaviour, 55, 875-882. https://doi.org/10.1006/anbe.1997.0668

Noël, M. V., Grant, J. W., & Carrigan, J. G. (2005). Effects of competitor-to-resource ratio on aggression and size variation within groups of convict cichlids. Animal Behaviour, 69, 1157-1163. https://doi.org/10.1016/j.anbehav.2004.07.019

Ottoni, E. B. (2000). EthoLog 2.2: A tool for the transcription and timing of behavior observation sessions. Behavior Research Methods, Instruments, & Computers, 32, 446-449. https://doi.org/10.3758/BF03200814

Øverli, Ø., Winberg, S., & Pottinger, T. G. (2005). Behavioral and neuroendocrine correlates of selection for stress responsiveness in rainbow trout-A review. Integrative and Comparative Biology, 45, 463-474. https://doi.org/10.1093/icb/45.3.463

Passos, C., Tassino, B., Loureiro, M., & Rosenthal, G. G. (2013). Intra-and intersexual selection on male body size in the annual killifish Austrolebias charrua. Behavioural Processes, 96, 20-26. https://doi.org/10.1016/j.beproc.2013.01.008

Phillips, C. T., & Johnston, C. E. (2008). Sound production and associated behaviors in Cyprinella galactura. Environmental Biology of Fishes, 82, 265-275. https://doi.org/10.1007/s10641-007-9279-5

Polverino, G., Cigliano, C., Nakayama, S., & Mehner, T. (2016). Emergence and development of personality over the ontogeny of fish in absence of environmental stress factors. Behavioral Ecology and Sociobiology, 70, 2027-2037. https://doi.org/10.1007/s00265-016-2206-z

Pruitt, J. N., & Keiser, C. N. (2014). The personality types of key catalytic individuals shape colonies' collective behaviour and success. Animal Behaviour, 93, 87-95. https://doi.org/10.1016/j.anbehav.2014.04.017

Raffinger, E., & Ladich, F. (2009). Acoustic threat displays and agonistic behaviour in the red-finned loach Yasuhikotakia modesta. Journal of Ethology, 27, 239-247. https://doi.org/10.1007/s10164-008-0109-9

Reddon, A. R., Balk, D., & Balshine, S. (2013). Probing aggressive motivation during territorial contests in a group-living cichlid fish. Behavioural Processes, 92, 47-51. https://doi.org/10.1016/j.beproc.2012.10.005

Roche, D. G., Careau, V., & Binning, S. A. (2016). Demystifying animal ‘personality’(or not): Why individual variation matters to experimental biologists. Journal of Experimental Biology, 219(24), 3832-3843. https://doi.org/10.1242/jeb.146712

Ruzzante, D. E., & Doyle, R. W. (1991). Rapid behavioral changes in medaka (Oryzias latipes) caused by selection for competitive and noncompetitive growth. Evolution, 45, 1936-1946. https://doi.org/10.1111/j.1558-5646.1991.tb02698.x

Réale, D., Reader, S. M., Sol, D., McDougall, P. T., & Dingemanse, N. J. (2007). Integrating animal temperament within ecology and evolution. Biological Reviews, 82, 291-318. https://doi.org/10.1111/j.1469-185X.2007.00010.x

Samaras, A., Dimitroglou, A., Sarropoulou, E., Papaharisis, L., Kottaras, L., & Pavlidis, M. (2016). Repeatability of cortisol stress response in the European sea bass (Dicentrarchus labrax) and transcription differences between individuals with divergent responses. Scientific Reports, 6, 34858. https://doi.org/10.1038/srep34858

Schneider, C. A., Rasband, W. S., & Eliceiri, K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nature Methods, 9, 671-675. https://doi.org/10.1038/nmeth.2089

Sih, A., Bell, A., & Johnson, J. C. (2004). Behavioral syndromes: An ecological and evolutionary overview. Trends in Ecology & Evolution, 19, 372-378. https://doi.org/10.1016/j.tree.2004.04.009

Sih, A., Chang, A. T., & Wey, T. W. (2014). Effects of behavioural type, social skill and the social environment on male mating success in water striders. Animal Behaviour, 94, 9-17. https://doi.org/10.1016/j.anbehav.2014.05.010

Sikkel, P. C., & Kramer, D. L. (2005). Territory revisits reduce intrusion during spawning trips by female yellowtail damselfish, Microspathodon chrysurus. Animal Behavior, 71, 71-78. https://doi.org/10.1016/j.anbehav.2005.03.028

Silva, A. C., Perrone, R., Zubizarreta, L., Batista, G., & Stoddard, P. K. (2013). Neuromodulation of the agonistic behavior in two species of weakly electric fish that display different types of aggression. Journal of Experimental Biology, 216, 2412-2420. https://doi.org/10.1242/jeb.082180

Slavík, O., Horký, P., Maciak, M., & Wackermannová, M. (2016). Familiarity, prior residency, resource availability and body mass as predictors of the movement activity of the European catfish. Journal of Ethology, 24, 23-30. https://doi.org/10.1007/s10164-015-0441-9

Smith, J. M., & Parker, G. A. (1976). The logic of asymmetric contests. Animal Behaviour, 24, 159-175.

Tanaka, T., Yoshida, M., Yokoo, H., Tomita, M., & Tanaka, M. (1998). Expression of aggression attenuates both stress-induced gastric ulcer formation and increases in noradrenaline release in the rat amygdala assessed by intracerebral microdialysis. Pharmacology, Biochemistry and Behavior, 59, 27-31. https://doi.org/10.1016/S0091-3057(97)00312-2

Tao, J., Little, R., Patetta, M., Truxillo, C., & Wolinger, R. (2002). Mixed the SAS System Course Notes. Cary, NC: SAS Institute Inc.

Tett, R. P., & Guterman, H. A. (2000). Situation trait relevance, trait expression, and cross-situational consistency: Testing a principle of trait activation. Journal of Research in Personality, 34, 397-423. https://doi.org/10.1006/jrpe.2000.2292

Tran, S., Nowicki, M., Fulcher, N., Chatterjee, D., & Gerlai, R. (2016). Interaction between handling induced stress and anxiolytic effects of ethanol in zebrafish: A behavioral and neurochemical analysis. Behavioural Brain Research, 298, 278-285. https://doi.org/10.1016/j.bbr.2015.10.061

Uher, J. (2011). Individual behavioral phenotypes: An integrative meta-theoretical framework. Why “behavioral syndromes” are not analogs of “personality”. Developmental Psychobiology, 53, 521-548. https://doi.org/10.1002/dev.20544

Ünver, B., & Kekilli, S. (2012). Reproduction biology of chub living in Lake Hafik. Iranian Journal of Fisheries Sciences, 11, 681-692.

Wackermannová, M. A., Horky, P., Amorim, M. C. P., & Fonseca, P. J. (2017). Computer-manipulated stimuli as a research tool in Mozambique tilapia Oreochromis mossambicus. Acta Ethologica, 20, 85-94. https://doi.org/10.1007/s10211-017-0252-9

Wagner, W. E. (1989). Graded aggressive signals in Blanchard's cricket frog: Vocal responses to opponent proximity and size. Animal Behaviour, 38(6), 1025-1038. https://doi.org/10.1016/S0003-3472(89)80141-1

Wisenden, B. D., Sailer, C. D., Radenic, S. J., & Sutrisno, R. (2011). Maternal inheritance and exploratory-boldness behavioural syndrome in zebrafish. Behaviour, 148, 1443-1456. https://doi.org/10.1163/156853911X616530

Wolf, M., & Weissing, F. J. (2012). Animal personalities: Consequences for ecology and evolution. Trends in Ecology & Evolution, 27, 452-461. https://doi.org/10.1016/j.tree.2012.05.001

Pupil size variation as a response to stress in European catfish and its application for social stress detection in albino conspecifics